Arabidopsis ACINUS is O-glycosylated and regulates transcription and alternative splicing of regulators of reproductive transitions.

Affiliation

Bi Y(1)(2), Deng Z(1), Ni W(3), Shrestha R(1), Savage D(1), Hartwig T(1), Patil S(1), Hong SH(1), Zhang Z(1), Oses-Prieto JA(4), Li KH(4), Quail PH(3), Burlingame AL(4), Xu SL(5), Wang ZY(6).
Author information:
(1)Department of Plant Biology, Carnegie Institution for Science, Stanford, CA, USA.
(2)Department of Biology, Stanford University, Stanford, CA, 94305, USA.
(3)Plant Gene Expression Center, United States Department of Agriculture/Agriculture Research Service, Albany, CA, USA.
(4)Department of Pharmaceutical Chemistry, University of California, San Francisco, San Francisco, CA, USA.
(5)Department of Plant Biology, Carnegie Institution for Science, Stanford, CA, USA. [Email]
(6)Department of Plant Biology, Carnegie Institution for Science, Stanford, CA, USA. [Email]

Abstract

O-GlcNAc modification plays important roles in metabolic regulation of cellular status. Two homologs of O-GlcNAc transferase, SECRET AGENT (SEC) and SPINDLY (SPY), which have O-GlcNAc and O-fucosyl transferase activities, respectively, are essential in Arabidopsis but have largely unknown cellular targets. Here we show that AtACINUS is O-GlcNAcylated and O-fucosylated and mediates regulation of transcription, alternative splicing (AS), and developmental transitions. Knocking-out both AtACINUS and its distant paralog AtPININ causes severe growth defects including dwarfism, delayed seed germination and flowering, and abscisic acid (ABA) hypersensitivity. Transcriptomic and protein-DNA/RNA interaction analyses demonstrate that AtACINUS represses transcription of the flowering repressor FLC and mediates AS of ABH1 and HAB1, two negative regulators of ABA signaling. Proteomic analyses show AtACINUS's O-GlcNAcylation, O-fucosylation, and association with splicing factors, chromatin remodelers, and transcriptional regulators. Some AtACINUS/AtPININ-dependent AS events are altered in the sec and spy mutants, demonstrating a function of O-glycosylation in regulating alternative RNA splicing.